Evidence map›Paper›PMID 31624345›Full record

ArticleThe ISME journal2020

Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids' di-symbiotic systems.

Alejandro Manzano-Marı N, Armelle Coeur d'acier, Anne-Laure Clamens, Céline Orvain, Corinne Cruaud, Valérie Barbe, Emmanuelle Jousselin

Open access · hybridAbstract read
In one paragraph

Article in The ISME journal, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 50 papers.

0numbers the graph read from it
0cells of the map it votes in
50citing papers in PubMed
13.3field-weighted citation impact, top 1% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

50 citing papers in PubMed, 114 citations in OpenAlex.

  1. Cellular remodeling of ovarian follicular epithelial cells transmits an obligate nutritional endosymbiont in a scale insect.Proceedings of the National Academy of Sciences of the United States of America · 2026
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  3. Plasmid mutation rates scale with copy number.Proceedings of the National Academy of Sciences of the United States of America · 2026
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  7. mSystems · 2025
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  8. Microorganisms · 2025
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  10. microRNA maintains nutrient homeostasis in the symbiont-host interaction.Proceedings of the National Academy of Sciences of the United States of America · 2024
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  14. Article
  15. Comparative genomics of a novelMicrobial genomics · 2024
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  16. Review
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4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

7 authors at 2 institutions in 1 country.

Alejandro Manzano-Marı NUMR 1062 Centre de Biologie pour la Gestion des Populations, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France. alejandro.manzano.marin@gmail.com.ORCID http://orcid.org/0000-0002-0707-9052
Armelle Coeur d'acierUMR 1062 Centre de Biologie pour la Gestion des Populations, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France.
Anne-Laure ClamensUMR 1062 Centre de Biologie pour la Gestion des Populations, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France.
Céline OrvainInstitut de Biologie François-Jacob, CEA, Genoscope, Évry Cedex, France.
Corinne CruaudInstitut de Biologie François-Jacob, CEA, Genoscope, Évry Cedex, France.
Valérie BarbeInstitut de Biologie François-Jacob, CEA, Genoscope, Évry Cedex, France.
Emmanuelle JousselinUMR 1062 Centre de Biologie pour la Gestion des Populations, INRA, CIRAD, IRD, Montpellier SupAgro, Univ. Montpellier, Montpellier, France.
Centre de Coopération Internationale en Recherche Agronomique pour le Développement · FRCommissariat à l'Énergie Atomique et aux Énergies Alternatives · FR

Funding

No grant is acknowledged in the PubMed record.

6 · The paper itself

Abstract

Many insects depend on obligate mutualistic bacteria to provide essential nutrients lacking from their diet. Most aphids, whose diet consists of phloem, rely on the bacterial endosymbiont Buchnera aphidicola to supply essential amino acids and B vitamins. However, in some aphid species, provision of these nutrients is partitioned between Buchnera and a younger bacterial partner, whose identity varies across aphid lineages. Little is known about the origin and the evolutionary stability of these di-symbiotic systems. It is also unclear whether the novel symbionts merely compensate for losses in Buchnera or carry new nutritional functions. Using whole-genome endosymbiont sequences of nine Cinara aphids that harbour an Erwinia-related symbiont to complement Buchnera, we show that the Erwinia association arose from a single event of symbiont lifestyle shift, from a free-living to an obligate intracellular one. This event resulted in drastic genome reduction, long-term genome stasis, and co-divergence with aphids. Fluorescence in situ hybridisation reveals that Erwinia inhabits its own bacteriocytes near Buchnera's. Altogether these results depict a scenario for the establishment of Erwinia as an obligate symbiont that mirrors Buchnera's. Additionally, we found that the Erwinia vitamin-biosynthetic genes not only compensate for Buchnera's deficiencies, but also provide a new nutritional function; whose genes have been horizontally acquired from a Sodalis-related bacterium. A subset of these genes have been subsequently transferred to a new Hamiltonella co-obligate symbiont in one specific Cinara lineage. These results show that the establishment and dynamics of multi-partner endosymbioses can be mediated by lateral gene transfers between co-ocurring symbionts.

Indexed as

Gene Transfer, HorizontalAnimalsAphidsBuchneraErwiniaSymbiosisVitaminsVitamins

Identifiers

PMID31624345
PMCPMC6908640
OpenAlexW2980902701

What OpenQuestion holds

Textmetadata
LicenceCC BY
Read underepoch 390

Registered trials

None linked

Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.